Biochar aging destabilizes viral-host mutualism and compromises the paddy methane sink

Biochar amendment is a promising strategy to mitigate methane emissions from rice paddies. However, the persistence of its benefit is often compromised by field aging, and the underlying microbial, particularly viral, mechanisms remain unclear. Using a decadal field experiment integrated with multi-omics, we show that biochar aging triggers a decisive shift in viral-host interactions within the methane-consuming microbiome. In fresh biochar-amended soil, temperate phages engage in a mutualism with keystone methanotrophs ( Methylomonas ), expressing auxiliary metabolic genes ( isc A, erp A) for iron-sulfur cluster assembly that potentiate methane oxidation—a classic Piggyback-the-Winner dynamic. In aged biochar, however, abiotic stressors drive a switch in viral life strategy from lysogeny to lytic replication, instigating a Kill-the-Stressed-Winner predation that dismantles the methanotroph population. Our study reveals that viral ecology governs the functional longevity of biochar, introducing a biological determinant to its climate efficacy. This underscores the critical need to incorporate viral dynamics into the design and assessment of agricultural carbon management strategies.